Phenotypic plasticity and diversity in insects plasticity and diversity in insects.pdfPhenotypic...

doi: 10.1098/rstb.2009.0263, 593-603365 2010 Phil. Trans. R. Soc. B

Armin P. Moczek Phenotypic plasticity and diversity in insects

Referenceshttp://rstb.royalsocietypublishing.org/content/365/1540/593.full.html#ref-list-1

This article cites 56 articles, 7 of which can be accessed free

Rapid responsehttp://rstb.royalsocietypublishing.org/letters/submit/royptb;365/1540/593

Respond to this article

Subject collections

(1387 articles)evolution (1158 articles)ecology

(139 articles)developmental biology (76 articles)systems biology

Articles on similar topics can be found in the following collections

Email alerting service hereright-hand corner of the article or click Receive free email alerts when new articles cite this article - sign up in the box at the top

http://rstb.royalsocietypublishing.org/subscriptions go to: Phil. Trans. R. Soc. BTo subscribe to

This journal is © 2010 The Royal Society

on January 29, 2010rstb.royalsocietypublishing.orgDownloaded from

http://rstb.royalsocietypublishing.org/content/365/1540/593.full.html#ref-list-1http://rstb.royalsocietypublishing.org/letters/submit/royptb;365/1540/593http://rstb.royalsocietypublishing.org/cgi/collection/systems_biologyhttp://rstb.royalsocietypublishing.org/cgi/collection/developmental_biologyhttp://rstb.royalsocietypublishing.org/cgi/collection/ecologyhttp://rstb.royalsocietypublishing.org/cgi/collection/evolutionhttp://rstb.royalsocietypublishing.org/cgi/alerts/ctalert?alertType=citedby&addAlert=cited_by&saveAlert=no&cited_by_criteria_resid=royptb;365/1540/593&return_type=article&return_url=http://rstb.royalsocietypublishing.org/content/365/1540/593.full.pdfhttp://rstb.royalsocietypublishing.org/subscriptionshttp://rstb.royalsocietypublishing.org/


Phil. Trans. R. Soc. B (2010) 365, 593–603

doi:10.1098/rstb.2009.0263

Review

*armin@

One concomplex

Phenotypic plasticity and diversityin insects

Armin P. Moczek*

Department of Biology, Indiana University, 915 East Third Street, Myers Hall 150,Bloomington, IN 47405-7107, USA

Phenotypic plasticity in general and polyphenic development in particular are thought to playimportant roles in organismal diversification and evolutionary innovation. Focusing on the evo-lutionary developmental biology of insects, and specifically that of horned beetles, I explore theavenues by which phenotypic plasticity and polyphenic development have mediated the origins ofnovelty and diversity. Specifically, I argue that phenotypic plasticity generates novel targets for evo-lutionary processes to act on, as well as brings about trade-offs during development and evolution,thereby diversifying evolutionary trajectories available to natural populations. Lastly, I examine thenotion that in those cases in which phenotypic plasticity is underlain by modularity in geneexpression, it results in a fundamental trade-off between degree of plasticity and mutation accumu-lation. On one hand, this trade-off limits the extent of plasticity that can be accommodated bymodularity of gene expression. On the other hand, it causes genes whose expression is specific torare environments to accumulate greater variation within species, providing the opportunity forfaster divergence and diversification between species, compared with genes expressed acrossenvironments. Phenotypic plasticity therefore contributes to organismal diversification on a varietyof levels of biological organization, thereby facilitating the evolution of novel traits, new species andcomplex life cycles.

Keywords: modularity; mutation accumulation; Onthophagus; relaxed selection

1. INTRODUCTION(a) Phenotypic plasticity—ubiquitous yet limitedVirtually all organisms as well as biological processesexhibit some degree of plasticity, that is, their functionis affected by external conditions (West-Eberhard2003). On one extreme, such effects may arise fromthe biochemical and biophysical dependencies ofbiological processes, such as the temperature depen-dency of enzymatic reactions or the pH-dependentfolding of proteins (Schlichting & Pigliucci 1995). Assuch, plasticity may be viewed as a by-product, anability that organisms did not have to evolve but thatcame for free as an emergent property of life givenhow life, in its simplest terms, works. On the otherextreme are highly choreographed responses toenvironmental changes such as acquired immunity,learning, nutrition-dependent modification of growthand reproduction or seasonal migration (Nijhout1999, 2003; West-Eberhard 2003). Here, plasticityrepresents a complex, evolved response to deal withimportant environmental changes, allowing organismsto maintain high fitness in the face of environmentalvariability (Schlichting & Pigliucci 1998). Importantly,such responses involve adjustments on not just one butmany levels of biological organization. For instance,

indiana.edu

tribution of 12 to a Theme Issue ‘From polyphenism tometazoan life cycles’.

593

the nutrition-dependent expression of different castesin social insects involves differences in geneexpression, endocrine physiology, regulation of append-age growth and development, development ofreproductive organs and behavioural repertoires(Wilson 1976; Wheeler & Nijhout 1983, 1984;Evans & Wheeler 1999, 2001a,b; Abouheif & Wray2002). What is less obvious is that much plasticityalso underlies many homeostatic responses and canal-ization in development (Scharloo 1991). Fromproducing constant blood sugar levels in the face ofnutritional variation to the generation of proper scalingrelationships of body parts during growth, organismsflexibly adjust a vast array of plastic processes onsome levels of biological organization to ensure pheno-typic constancy on others (Scharloo 1991; Dworkin2005).

Despite the obvious adaptive significance of plas-ticity, it is clearly not without limits and apparentconstraints. Organisms are not infinitely plastic andinstead limited in the range of environments they canrespond to. Even in the most extreme cases such aspolyphenisms, expression of alternative phenotypes isalmost always restricted to two morphs rather thanfive or eight, even though one could probably make acase that such hypothetical alternatives should dowell in at least some environments (West-Eberhard2003). The notable exceptions are social castes in theHymenoptera (Hölldobler & Wilson 1990), a case wewill later on return to. Lastly, it is worth noting that

This journal is q 2010 The Royal Society

mailto:[email protected]://rstb.royalsocietypublishing.org/

594 A. P. Moczek Review. Plasticity and diversity in insects


plasticity, central as it is to life on this planet includ-ing our own, also plays a central role in manyimportant human diseases. From autoimmune dis-eases to obesity, many of our ‘modern’ diseasesinvolve plasticity gone wrong, bringing about inap-propriate responses to external changes (Gilbert &Epel 2009).

In this review, I will explore how plasticity contrib-utes to organismal diversification as well as the costsand limits of this contribution. Drawing from theinsect literature, and specifically from recent work onhorned beetles, I will highlight avenues by which plas-ticity and its developmental and genetic underpinningsdiversify evolutionary trajectories available to evolvinglineages. I will begin by introducing my focal taxa,the insects, and within them, the horned beetles,as particularly illuminating macro- and microcosmsfor understanding the causes, mechanisms andconsequences of plasticity.

(b) Insect biology and the rangeand power of plasticity

If an alien life form would visit planet Earth with themission to identify the group of multicellular organ-isms that has diversified most successfully, it wouldselect, without doubt, the insects. Insects representover one million of the roughly 1.4 million speciesnamed thus far. Insects have evolved every imaginablefeeding habit and colonized nearly every imaginableecological niche with the remarkable exception ofmarine habitats (Grimaldi & Engel 2005). Muchof this diversity is contributed by holometabolousinsects, represented by nine insect orders that featurecomplete metamorphosis and a pupal stage interca-lated between larvae and adults (Yang 2001). Allsuperdiverse insect orders (Lepidoptera, Diptera,Hymenoptera, Coleoptera) are holometabolous.Combined, these four orders alone account for over750 000 species and thus about three-quarters of allnamed insects and more than half of all living species.Among them, the beetles stand out the most, account-ing for every fourth named species on this planet(Grimaldi & Engel 2005).

Evolution of holometabolous development andmetamorphosis decoupled larval and adult stagesand permitted larvae and adult versions of the sameanimal to specialize in often very different niches,feeding modes and habitats (Jacobs & Renner 1988).The life-stage diversity mediated by holometabolousdevelopment is truly spectacular and a remarkabletestament to the phenotypic diversity and disparity,including morphological, physiological and behaviour-al traits, which can be accommodated by a singlegenome. More importantly, it is also testament to theincredible plasticity of development, which if giventhe proper genetic and environmental cues can trans-form a maggot into a fly, a caterpillar into a mothand a grub into a beetle.

Insects also stand out as exemplars of cases in whichalternative phenotypes are not expressed sequentially,as in larval and adult stages, but simultaneously, asin the context of polyphenisms (Nijhout 2003).Some of the most spectacular cases of polyphenic

Phil. Trans. R. Soc. B (2010)

alternatives are found among insects, including socialcastes in the Hymenoptera, termites and aphids(Lüscher 1960; Wheeler & Nijhout 1983; Stern &Foster 1996), seasonal polyphenisms in butterflies(Shapiro 1976), dispersal polyphenisms (Zera &Denno 1997), alternative asexual and sexual reproduc-tive phases in aphids (Moran 1991) and alternativemale morphologies in thrips (Crespi 1988) and beetles(Emlen 1994). Here again, a single genome displaystremendous ability to accommodate a wide range ofoften highly disparate phenotypes in response tochanges in external conditions. Furthermore, inmany cases, phenotypic differences between alterna-tives mirror major macro-evolutionary transitionssuch as the alternation between asexual and sexualstages in aphids or wingless and winged stages insocial insects (West-Eberhard 2003).

Insects thus emerge as a taxon that combines tre-mendous diversity and species richness withremarkable plasticity in development. This leads tothe main question that this review hopes to address:did this exuberant species richness and diversityevolve independently of, in spite of, or possiblybecause of the level of plasticity observed within theinsects? Before addressing this question, I wouldbriefly like to introduce a group of insects that is begin-ning to emerge as a particularly useful microcosm forstudying the interplay between plasticity, developmentand evolution, and for evaluating the creative potentialof phenotypic plasticity: the horned beetles.

(c) Horned beetles: a microcosm forunderstanding the causes, mechanisms

and consequences of plasticity

Horned beetles are not a taxonomic entity. Instead,they exist as a group simply because of biologists’interests in, and at times obsessions for, beetles withexaggerated and often bizarre secondary sexual traits(figure 1). Beetle species belonging to at least sixfamilies have evolved horn-like structures (reviewedin Snell-Rood & Moczek in press), though the mostextreme and diverse cases all exist within one of themost species-rich families of beetles, the Scarabaeidae(figure 1). This family is home to the spectacular sub-family Dynastinae, including the southeast Asiangenus Chalcosoma that enchanted Darwin, and thesubfamily Scarabaeinae, home to all true dung beetles(Darwin 1871; Arrow 1951; Balthasar 1963).

Horned beetles have fascinated biologists for anumber of reasons (reviewed in Moczek 2005). First,beetle horns are spectacular traits, enormous in sizeand often bizarre in shape. Furthermore, beetlehorns attract attention because of the fantastic diver-sity that exists between and within species. Betweenspecies, horns differ in size, location, number andshape. Intriguingly, all of these types of variation canalso be found within species, in the context of sexualdimorphisms (females commonly lack or have greatlyreduced horns) as well as male dimorphism. Thislatter level of variation is especially noteworthy as itreflects diversity in male phenotypes produced inresponse to variation in larval nutrition rather thanallelic differences between males. In extreme cases,

http://rstb.royalsocietypublishing.org/

(a) (b) (c)

(e) (d )

Figure 1. Examples of horned beetles illustrating diversity and magnitude of horn expression in adult beetles: (a) Phanaeusimperator, (b) Eupatorus gracilicornis, (c) Onthophagus watanabei, (d) Golofa claviger and (e) Trypoxylus (Allomyrina) dichotoma.

Review. Plasticity and diversity in insects A. P. Moczek 595


the resulting variation is discrete, causing males to fallinto distinct alternative morphs. In such cases, alterna-tive male morphs often not only differ in their relativeinvestment into horns, but also display alternativereproductive behaviours (Moczek & Emlen 2000),differential genitalic investment (Simmons & Emlen2006; Parzer & Moczek 2008), thermoregulation(Shepherd et al. 2008), differences in brain proteinexpression (Y. Yerushalmi & A. Moczek 2009, unpub-lished data), etc. Lastly, beetle horns lack clearhomology to other structures in beetles or in otherinsect orders. Horns are not merely modified legs orantennae; instead, they exist alongside these structuresand can therefore be interpreted as an example of anevolutionary novelty, invented at some point duringbeetle history (Moczek et al. 2006). Hence, beetlehorns have become the focus of studies interestedin the early stages of organismal innovation, and thegenetic, developmental and ecological mechanismsthat mediate the origin of novelty from within theconfines of ancestral homology.

In all these aspects, one genus of horned beetlesstands out: Onthophagus. This genus is, with an esti-mated 2400 extant species, the most speciose genusin the animal kingdom (Balthasar 1963; Matthews1972; Howden & Young 1981). It combines incrediblespecies richness with dramatic diversity in theexpression of horns, and as we will see in §2important components of this diversity are linkedone way or another to phenotypic plasticity. We thusarrive again at the central question that this review istrying to address: did the amazing species richnessand diversity seen in horned beetles in general, andthe genus Onthophagus in particular, evolve indepen-dently of, in spite of, or because of the level ofplasticity observed in these taxa?


2. PHENOTYPIC PLASTICITY AND ORGANISMALDIVERSIFICATIONPhenotypic plasticity has been postulated to be bothan inhibitor and a facilitator of phenotypic diversifica-tion (Schlichting & Pigliucci 1998; Pigliucci 2001).Conflicting viewpoints on the issue arise for anumber of reasons, for instance, whether organismaldiversity is equivalent to species richness, or whetherother proxies might be more appropriate. For example,plasticity permits organisms to adjust to a range ofenvironmental conditions, and as such may eliminatepopulation subdivision arising from environmentalheterogeneity, which otherwise might facilitate theevolution of specialist species. In this case, plasticitymay be viewed as reducing organismal diversity becauseit prevents speciation. However, if species richness isnot used as a proxy for organismal diversity, thesame argument can actually be used to supportthe opposite claim. By permitting the evolution ofenvironment-specific responses in phenotype expression,phenotypic plasticity permits organismal diversificationwithin species, such as alternative morphs, withouthaving to couple it to speciation. Here, phenotypic plas-ticity permits an increase in phenotypic diversitywithout a commensurate increase in species richness.

Another general, and related, argument for andagainst a contribution of plasticity to organismal diver-sification emphasizes its role in population extinction.Here, conflicting viewpoints arise primarily owing todifferences in the time frame over which plasticity’scontribution is evaluated. Both start with the obser-vation that plasticity reduces the likelihood ofextinctions in the face of environmental heterogeneity.If environmental changes, such as global climatechange or the appearance of habitat bridges, causenew niches to become available for colonization,




phenotypic plasticity may predispose plastic species tobe successful colonizers, reducing the likelihood ofnew, specialized species to invade or evolve. Overthis short time frame, plasticity would permit habitatexpansion but without leading to a net increase inspecies diversity. At the same time, by bufferingpopulations against extinctions owing to environ-mental fluctuations, plasticity can be viewed asmaintaining phenotypic diversity despite exposure tonew conditions with novel environmental challenges.By preventing population extinctions, plasticity nowdramatically extends the opportunity for phenotypicdifferentiation to evolve subsequently, includingspeciation (West-Eberhard 2003).

In the remainder of this review, I argue that eventhough these general considerations all capture impor-tant aspects of plasticity’s role in evolution, plasticity’scontribution to organismal diversification, includingspeciation, goes well beyond. Instead, rather thanmerely increasing phenotypic diversity within speciesor preserving the opportunity for diversification tooccur by preventing extinctions, I argue below thatplasticity itself opens up opportunities for diversifica-tion, including speciation, that would not existotherwise.

(a) Phenotypic plasticity provides novel targetsfor evolutionary processes

Adaptive phenotypic plasticity, as in the case of poly-phenisms, involves the acquisition of information onenvironmental conditions and the correspondingadjustment of genetic, developmental, physiologicaland/or behavioural phenotypes. Responses to environ-mental changes may range from gradual, with one‘unit’ of environmental change soliciting a more orless corresponding unit of phenotypic adjustment, todiscrete, with a threshold separating phenotypes pro-duced under one range of conditions from thoseproduced under another. Numerous studies havenow shown that both nature (e.g. gradual versus dis-crete) and magnitude (e.g. small or large changesacross environments) of plastic responses can evolveindependently of other aspects of the phenotype. Forexample, lacewings and pitcher plant mosquitoes(Tauber & Tauber 1972; Bradshaw et al. 2003) exhibitheritable variation for the photoperiodic responsethreshold underlying the facultative expression of dia-pause, families of cabbage-white butterflies showheritable variation for the ability to adjust host-plantpreferences (Snell-Rood & Papaj 2009), and speciesof ants and termites differ, at times dramatically, inthe relative size cutoffs for different nutrition-determined castes that coexist in a colony (Wilson1953; Hölldobler & Wilson 1990). Nature and magni-tude of responses to environmental variation thereforecontribute to the trait repertoire of a population thatis subject to evolutionary processes, and that cancontribute to evolutionary diversification betweenpopulations and species.

Studies on horned beetles have provided additionalinsights into the dynamics and consequences of plas-ticity evolution. Male horned beetles in the genusOnthophagus often exhibit species-specific differences


in the exact scaling relationship between body sizeand horn length (reviewed in Emlen 2000; Moczek2005). In all Onthophagus species, adult body size isheavily influenced by nutritional conditions experi-enced during larval development, and the relativesizes of other traits, such as horns, are adjusted accord-ingly: larvae with access to good feeding conditionswill metamorphose into large adults with relativelylarge horns, whereas larvae with access to suboptimalconditions will give rise to small adults with relativelysmall horns. While this holds true for all Onthophagusspecies studied to date, the exact relationship betweennutrition-determined body size and the correspondinghorn size exhibits remarkable interspecific differences,causing body size–horn length scaling relationships torange from linear to ‘broken’ to sigmoidal (figure 2a).In all these cases, species adjust horn expression rela-tive to nutritional variation, but the exact nature andmagnitude of adjustments has undergone dramaticdiversification independently of horn expressionper se. Studies in the field and laboratory on one par-ticular species now provide the first insights into themechanisms, dynamics and consequences of plasticityevolution in nature.

Onthophagus taurus is a species native to the Medi-terranean, which became introduced to the EasternUSA as well as to Eastern and Western Australia inthe early 1970s (Moczek 2003). Males in this speciesexhibit a pronounced sigmoidal scaling relationshipbetween body size and horn length, causing malesbelow a certain size threshold to remain largely horn-less and males above to express a pair of long,curved head horns. Comparisons of archival museumcollections with present-day populations documentedthat introduced populations diverged in less than40 years from their Mediterranean ancestors in thebody size threshold that separates alternative malemorphs to a degree normally only observed betweenspecies (figure 2b(ii)(iii); Moczek & Nijhout 2003).A combination of field and laboratory studies providedevidence consistent with the hypothesis that thesedivergences were driven by selection acting on hornlength–body size thresholds, adjusting them to thelocal competitive conditions in which horned (fighting)and hornless (sneaking) males perform (Moczek2003). Divergences are maintained over generationsunder a common garden regime, suggesting that theobserved divergences indeed reflect heritable changesin the developmental machinery underlying nutri-tion-dependent morph expression (Moczek et al.2002). In this example, plasticity in horn developmenthas opened up traits, such as the body size threshold,for selection to act on, allowing populations tosubstantially diverge in threshold values in an extra-ordinarily short time period without diverging inthe average phenotypes of horned and hornless malemorphs, which instead are largely indistinguishableacross populations (Pizzo et al. 2008).

Findings such as these illustrate that the genetic anddevelopmental basis of plasticity in trait expressionmust at least in part be separate from, and indepen-dent of, the genetic and developmental basis of traitexpression per se. For instance, earlier work on theendocrine regulation of horn expression in O. taurus


8

(i)

(ii)

(iii)

9 10 11 12 3 4 5 6 7 8

6

4

2

0

4

3

2

1

0

4

3

2

1

05.55.04.55.04.5

0

1

2

3

4

0

1

2

horn

leng

th (

mm

) horn length (mm

)

body size (mm) body size (mm)

2

4

6

8

10

(a) (b)

5.5

(i)

(ii)

(iii)

Figure 2. Examples of (a) complex-scaling relationships and (b) divergences in scaling relationships in horned beetles. (a)Examples of horn length–body size scaling relationships in the beetle genus Onthophagus: (i) linear scaling relationship ofpaired head horns in O. watanabei (males: open circles; females: open diamonds); (ii) broken scaling relationship of pronotalhorn length in male O. binodis; (iii) S-shaped (sigmoidal) scaling relationship of paired head horns in male O. taurus (modifiedafter Moczek 2009). (b) Examples of divergences in scaling relationships in the genus Onthophagus over a range of phylogeneticdistances: (i) three Onthophagus species, which diverged approximately 20–38 Myr ago (O. taurus: open circles; O. nigriventris:solid diamonds; O. gazella: open triangles); (ii) divergences in scaling relationships between two sister species, O. taurus (opencircles) and O. illyricus (solid circles), which diverged approximately 10 000 years ago (Pizzo et al. 2008); (iii) divergences inscaling relationships between three allopatric O. taurus populations established less than 40 years ago from a commonMediterranean ancestor (Eastern USA: open circles; Eastern Australia: grey circles; Western Australia: solid circles; modifiedafter Moczek 2003).



showed that a common insect hormone, juvenile hor-mone (JH), appears to regulate horn expression inmale beetles. Males fated to develop into hornlessmales will express horns if treated with certain dosagesof JH analogues during a certain sensitive period(Emlen & Nijhout 1999). Follow-up studies on thedivergent O. taurus populations introduced abovethen showed that threshold divergences appeared tohave been made possible developmentally by evolvedchanges in the degree and timing of sensitivity to JH.The Western Australian population, which inducehorn expression only at very large male body sizes,required substantially higher JH dosages during laterlarval development to induce horns in presumptivehornless males compared with Eastern USA males


(Moczek & Nijhout 2002). Clearly, evolutionarychanges in JH-mediated threshold determination canoccur independently of evolutionary changes—orstasis—in other aspects of horn expression.

That said, the same studies also showed that diver-gences in the JH-mediated underpinnings of body sizethresholds did not come entirely for free; instead, theyappeared to have been accompanied by correlatedchanges in other traits unrelated to horn expression,in particular the length of larval development andthe timing of metamorphosis. Specifically, researchersobserved that populations that limit horn expression toonly the largest males also exhibited an increase in thelength of the last larval instar (but not earlier instars)and the timing of the larval-to-pupal moult (but not




other moults), and hypothesized that these correlateddifferences may have a common root in JH’s role inthe regulation of moulting and metamorphosis,which constitutes one of its most basic, and ancestral,functions during the development of holometabolousinsects (Moczek & Nijhout 2002). Specifically, thepresence or absence of JH during critical periods pre-ceding each moult determines whether moults maintainthe same identity (JH present), as in a larval-to-larvalmoult, or change identity (JH absent), as in a larval-to-pupal or pupal-to-adult moult (Nijhout 1994). JHtherefore has to be cleared from the haemolymph oflate O. taurus larvae in order for them to transit tothe pupal stage, which may be in conflict with the rela-tively high JH titers required immediately prior to thisperiod to induce horns in large males. Current modelstherefore postulate that raising body size threshold tolarger body sizes via delaying the sensitive period forJH and increasing JH titres required for horn inductionshould delay the complete removal of JH from larvalhaemolymph, and therefore bring about an extensionof the last larval instar and a corresponding delay ofthe larval–pupal moult (Moczek & Nijhout 2002).While this scenario remains to be verified experimen-tally, these observations nevertheless begin tointroduce an important new aspect in plasticity’s rolein organismal diversification: not only does plasticityprovide new targets for evolutionary processes to acton that would otherwise not exist, but plasticity evo-lution may also bring about correlated changes inother traits that may not be possible in differentcontexts. Correlated changes in other traits are import-ant in this context because they constitute a criticalsource of trade-offs in development and evolution.As we will see in the next section, evolutionary changesin components of plasticity can result in particularlyinteresting, and often non-intuitive, trade-offs withother traits, with the ability to bias evolutionary trajec-tories and patterns of phenotypic diversification indescendant lineages.

(b) Phenotypic plasticity creates noveltrade-offs

At the most basic level, trade-offs during developmentmay arise when two or more structures or developmen-tal processes compete for a shared and limited pool ofresources to sustain their growth or operation(Klingenberg & Nijhout 1998; Nijhout & Emlen1998). Increased investment into one structure or pro-cess may only then be possible through decreasedinvestment in another. The resulting resource allo-cation trade-offs not only have the ability to alterdevelopmental outcomes but may also bias evolution-ary trajectories available to descendant lineages.Resource allocation trade-offs are probably ubiquitousin the Metazoa, but appear particularly important inthe development of holometabolous insects. Here,most growth of adult structures is restricted to a timeperiod during which pupae represent a closed system,i.e. are no longer taking in nutrients and instead fuelmost of metamorphosis using a finite pool of storedresources.

Resource allocation trade-offs can of course occurindependently of the degree of plasticity associated


with a given set of traits, i.e. should not be restrictedto plastic traits, or processes underlying aspects ofplasticity. However, recent work suggests that plastictrait expression can contribute trade-offs that wouldotherwise not occur. For instance, cabbage-white but-terflies differ heritably in their ability to learn noveloviposition host plants (Snell-Rood & Papaj 2009).While learning is adaptive under at least some environ-mental conditions, it carries costs with it. Interestingly,some of these costs, such as investment in early mush-room-body development and overall brain size, arefixed, i.e. are incurred during development regardlessof whether learning in life occurs or not. In contrast,other costs such as mushroom-body differentiationlater in adult life are facultative and are only incurredif learning actually takes place (Snell-Rood et al.2009). Importantly, learning-associated investmentinto brain development traded off with reproductiveinvestment measured as the number of matureeggs at emergence (Snell-Rood et al. in press b).Simmons & Emlen (2006) reported a similar trade-off in Onthophagus beetles, where they documented anegative correlation between the degree of plasticityin horn expression and investment into testis; however,the mechanisms underlying this trade-off remainobscure.

Aspects of plastic trait expression other than just therange of plasticity may also participate in trade-offswith other traits. A recent study on 10 Onthophagusspecies and four divergent O. taurus populations illus-trates that evolutionary changes in threshold body sizesthat separate alternative horned and hornless malemorphs are associated with substantial trade-offs inthe expression of other traits (Parzer & Moczek2008). Earlier experimental work had shown thatmales that had their genital precursor cells removedduring larval development, and thus were unable todevelop copulatory organs, expressed significantlylarger horns than untreated or sham-treated males(Moczek & Nijhout 2004). By showing that structureswhich develop at the opposite ends of an animal canengage in significant trade-offs, this study contradicteda common notion at the time that trade-off intensityshould decay with distance. More importantly, how-ever, it sets the stage for a series of comparativestudies investigating whether corresponding trade-offsignatures also exist in nature. Investigating threeexotic (figure 2b(iii)) and one native populations ofO. taurus, Parzer & Moczek (2008) showed that indu-cing horn expression at relatively smaller body sizes(as in Eastern USA males) correlates with reducedinvestment into male copulatory organs (figure 3a,b).Delaying horn expression to relatively larger bodysizes (as in Western Australian males) had the oppositeeffect and resulted in increased investment intocopulatory organs. Recall that threshold divergencesbetween exotic populations evolved in less than40 years since introduction from a common ancestor,and were apparently driven by selection acting onhorn length–body size thresholds (Moczek 2003).If correct, this suggests that evolutionary changesin copulatory organ size occurred as a secondaryby-product of selection operating on aspects of plas-ticity in secondary sexual trait expression. Replicating


0.004

(a)

(b)

(c)

–0.003

–0.010

0 0.1 0.20.2

0

–0.2

–2 0 2 4

relative investment into horns

rela

tive

inve

stm

ent i

nto

copu

lato

ry o

rgan

rela

tive

inve

stm

ent i

nto

copu

lato

ry o

rgan

0.3

Figure 3. Trade-offs between investment into polyphenicexpression of horns and canalized investment into copulatoryorgans in populations and species of Onthophagus beetles. (a)Horned male Onthophagus taurus. Arrows highlight hornsand copulatory organ. (b) Relative investment into copula-tory organ size as a function of relative investment intopolyphenic horn expression in four different populations ofO. taurus. Error bars represent one standard error. (c) Rela-tive investment into copulatory organ size as a function ofrelative investment into horn size in 10 different Onthophagusspecies. Data are corrected for differences in body size.Modified after Parzer & Moczek (2008).



this approach across 10 Onthophagus species that havediverged from each other between 10 000 years and 38Myr ago revealed a similarly strong trade-off signature(figure 3c; Parzer & Moczek 2008). Combined, thesefindings suggest that trade-offs between aspects ofhorn polyphenisms and copulatory organ developmentalready characterize interpopulational divergences butcontinue to shape morphological diversification wellafter speciation is complete. The implication of copu-latory organ size in this trade-off is of particularsignificance because evolutionary changes in malecopulatory organs are thought to play a major role inthe early evolution of reproductive isolation in insects(Eberhard 1985; Eberhard et al. 1998). It is typicalfor cryptic or recent insect species to be only


distinguishable by copulatory organ morphology,suggesting that whatever mechanism is able to influ-ence copulatory organ expression in a givenpopulation may have immediate consequences forthat population’s ability to interbreed with others.Given the importance of copulatory organ morphologyfor reproductive isolation, the findings outlined abovebegin to raise the possibility that horn plasticity evo-lution may have the ability to promote speciation asa by-product. If trade-offs between components ofhorn plasticity and male copulatory organs areindeed driving speciation in Onthophagus, this wouldhelp explain how onthophagine beetles succeeded toevolve into a genus famous for both exuberant diver-sity in horn expression and remarkable speciesrichness (Arrow 1951; Matthews 1972).

More generally, the examples listed above illustratethat just as plasticity can contribute novel targets forevolutionary processes to act on, it can help generatenovel types of trade-offs that influence morphological,physiological or behavioural trait expression elsewherein the same individual. On one hand, plasticity maytherefore constrain and limit evolutionary trajectoriesavailable to lineages. On the other hand, such con-straints may force lineages to explore phenotypic,and corresponding ecological, space that otherwisemay remain unexplored. Similarly, trade-offs maycause populations and species to diverge in manymore traits than just those selection may be targeting.As such, plasticity-associated trade-offs represent bothconstraints on and opportunities for organismal diver-sification. We will see the same two themes re-emergein the next section, when we explore some of thegenetic mechanisms of plasticity, and their emergentproperties for plasticity evolution.

(c) Phenotypic plasticity increases geneticvariation and divergence—the mutation-

modularity trade-off hypothesis

The nature of the genetic basis of plasticity has beenthe subject of an intense debate (Via et al. 1995). Agrowing number of studies have now shown that plas-ticity, including polyphenic development, is oftenunderlain by modularity in gene expression, i.e. differ-ent environmental conditions and phenotypes areassociated with the expression of very different suitesof genes (Hymenoptera: Evans & Wheeler 2001a,b;Pereboom et al. 2005; Judice et al. 2006; Donnell &Strand 2006; Isoptera: Scharf et al. 2003; Hojo et al.2005; Hoffman & Goodisman 2007; Hemiptera:Kutsukake et al. 2004; Onthophagus: Snell-Rood et al.in press a). In such cases, the frequency by which agiven suite of genes, or module, becomes expressedin a population within a given generation, and thus vis-ible to selection, becomes a function of the frequencyof the inducing environmental conditions. Rare con-ditions affecting gene expression either only in everycouple of generations or only in a subset of individualswithin a population cause genes specific to them to behidden from selection and thus free to accumulate alarger number of mutations relative to genes expressedin every individual in every generation. Recent empiri-cal and theoretical work (Van Dyken & Wade, in press;




Snell-Rood et al. in press a) suggests that relaxed selec-tion resulting from modularity in gene expressiondrives a fundamental trade-off between mutationaccumulation and the degree of modularity in geneexpression underlying plastic responses to environ-mental changes. If correct, this trade-off hasfar-reaching implications for defining the costs, limitsand evolutionary consequences of plasticity.

The notion that certain restrictions in geneexpression can result in relaxed selection permittingmutation accumulation has been proposed and exam-ined previously in contexts outside phenotypicplasticity, such as the evolution of senescence(Charlesworth 1994) and the biology of niche conser-vativism (Holt 1996, see Snell-Rood et al. in press a foradditional examples). In each case, genes whoseexpression is restricted to a subset of individuals ineach generation are predicted to experience relaxedselection and accumulate mutations more quickly rela-tive to similar genes expressed in every individual.Work on maternal effect genes has now brought theconcept closer to developmental genetics and modu-larity in gene networks. Moreover, it has provided afirst critical juxtaposition of empirical data with pre-dictions from population-genetic models. Maternaleffect genes are genes transcribed by mothers, whichthen incorporate transcripts or their protein productsinto their eggs. Strict maternal effect genes are onlyexpressed by females and only function during earlyembryogenesis. Even though fathers possess the corres-ponding genes, they are not expressed during their lifetime. As such, only half of a given population expressesa given strict maternal effect gene, assuming a 1 : 1 sexratio, reducing the efficiency of selection for suchgenes relative to those expressed in every individual,or the so-called zygotic genes. Population genetictheory predicts that given the halving in the numberof expressed copies, maternal effect genes shouldaccumulate twice the mutation load within popu-lations compared with similar zygotic genes (Wade1998). Theory furthermore predicts that providednucleotide substitutions have at least mildly deleter-ious fitness effects, maternal effect genes have thepotential to diverge many times faster between speciesthan corresponding zygotic genes (Demuth & Wade2007). Both predictions are now matched by empiricaldata (Barker et al. 2005; Demuth & Wade 2007;Cruickshank & Wade 2008). In the most extensivestudy, Cruickshank & Wade (2008) examinedsequence variation within and between species ofDrosophila of 39 genes instrumental for early embry-onic development including 9 strict maternal effectgenes and 30 zygotically expressed genes. As pre-dicted, they found sequence variation within species(D. melanogaster) to be two- to threefold higher formaternal-effect genes than any other gene class, andsequence divergences between species (D. melanogasterand D. simulans) to be two- to fourfold higher inmaternal effect genes than any other gene class.Combined, these data provide compelling supportfor the hypothesis that relaxed selection acting onmaternal-effect genes causes increased sequence vari-ation within species, in turn fuelling more rapiddivergences between species.


This body of work focused primarily on modularityof gene expression as it arises during early embryonicdevelopment via the partitioning of gene expressioninto maternal effect versus zygotic genes. However,its theoretical foundation and predictions can easilybe applied to modularity in gene expression arisingthrough plasticity: genes induced in individuals experi-encing rare environments should exhibit reducedselection, permitting accumulation of greater sequencediversity within species and creating the potential formore rapid divergence between species relative tosimilar genes expressed in every individual in everygeneration (Snell-Rood et al. in press a). Recentwork on bacterial quorum-sensing genes, which areinduced only in generations exposed to certain popu-lation densities, provides support for both predictions(Van Dyken & Wade, in press). Current studies onhorned beetles are now seeking to apply the sameframework to polyphenic insects. Specifically, the recentdevelopment of genomic resources for Onthophagusbeetles has permitted the identification of geneswhose expression is specific to horned or hornlessmale morphs, or shared between morphs or sexes. Sur-veys of sequence variation within and between speciesare now under way to determine whether morph-specific genes harbour greater levels of within-speciesnucleotide diversity and diverge faster between speciesthan similar morph-shared genes. Preliminary data ona small number of gene pairs are consistent with thesepredictions, but it remains to be seen whether this willemerge as a general pattern (E. C. Snell-Rood & A.Moczek 2009, unpublished data). If so, acceleratedevolution in modular plasticity genes relative to consti-tutively expressed genes would have far-reachingconsequences for our understanding of the costs,limits and consequences of modular plasticity.

For example, by virtue of accelerating mutationaccumulation and divergence, genes underlying modu-lar plasticity may be more likely to evolve newfunctions compared with similar non-plastic genes.If correct, plasticity genes may be predisposed tocontribute disproportionally to sub- and neo-functionalization events during organismal evolution(Demuth & Wade 2007; Cruickshank & Wade2008). By the same argument, however, acceleratedmutation accumulation may render modular plasticitygenes more prone to acquire deleterious mutations andevolve into pseudogenes. This should be more pro-nounced in modules that are expressed rarely whencompared with more commonly induced modules,and as such may place an upper limit on the range ofplasticity that can be accommodated through modularplasticity: modules whose expression occurs too infre-quently may simply suffer too many mutations to befunctionally maintainable within populations (Snell-Rood et al. in press a). It is interesting to speculatewhether it is due to relaxed selection and mutationaccumulation that most polyphenisms are limited tothe expression of two alternative morphs, with the con-spicuous exception of castes in social insects. Here,colony-level selection, a level of selection absent innon-social insect polyphenisms, may provide an effec-tive mechanism limiting mutation accumulation incaste-specific genes, permitting the maintenance of




more than two discrete castes (Snell-Rood et al.in press a). Lastly, even though relaxed selection mayimpose constraints on the range of plasticity that canbe accommodated through modularity in geneexpression, it may at the same time create opportu-nities for alternative genetic underpinnings ofplasticity to evolve, such as integrated networkswhere the same suites of genes, but via altered typesof interactions, contribute to the expression of differ-ent phenotypes in different environments. Whilemany of these implications, though fundamental, areclearly speculative at this point, recent methodologicaland theoretical advances promise that criticalempirical evaluations will follow soon.

3. CONCLUSIONSPhenotypic plasticity and polyphenic developmentcontribute to organismal diversification on a varietyof levels of biological organization. On one level,phenotypic plasticity contributes traits such as devel-opmental thresholds and switches for evolutionaryprocesses to act on. Evolutionary changes in suchtraits may contribute to organismal diversification,including speciation, without changes in traitexpression per se. Similarly, evolutionary changes inpolyphenic development can bring about correlatedchanges in other traits, in turn increasing the possi-bility for trade-offs to shape subsequent patterns ofdiversification. Lastly, the mutation-modularitytrade-off hypothesis provides a plausible mechanismexplaining how modularity in gene expression under-lying plasticity can result in relaxed selection andincreased mutation accumulation in highly modulargenes, with the potential to contribute to both theevolutionary range and limits of modular phenotypicplasticity.

Tami Cruickshank and Emilie Snell-Rood provided helpfulcomments on earlier drafts of this chapter. Researchpresented here was supported by National ScienceFoundation grants IOS 0445661 and IOS 0718522.

REFERENCESAbouheif, E. & Wray, G. A. 2002 Evolution of the gene net-

work underlying wing polyphenism in ants. Science 297,249–252. (doi:10.1126/science.1071468)

Arrow, G. H. 1951 Horned beetles. The Hague, The Nether-lands: Junk.

Balthasar, V. 1963 Monographie der Scarabaeidae undAphodiidae der palaearktischen und orientalischen Region(Coleoptera: Lamellicornia). Band 2, Coprinae. Prag:Verlag der tschechoslowakischen Akademie derWissenschaften.

Barker, M. S., Demuth, J. P. & Wade, M. J. 2005 Maternalexpression relaxes constraint on innovation of the anteriordeterminant, bicoid. PloS Genet. 1, 527–530. (doi:10.1371/journal.pgen.0010057)

Bradshaw, W. E., Quebodeaux, M. C. & Holzapfel, C. M.

2003 Circadian rhythmicity and photoperiodism in thepitcher-plant mosquito: adaptive rsponse to the photicenvironment or correlated response to climatic adap-tation? Am. Nat. 161, 735–748. (doi:10.1086/374344)

Charlesworth, B. 1994 Evolution in age-structured popu-lations. Camb. Stud. Math. Biol. 13, 1–306.


Crespi, B. J. 1988 Adaptation, compromise and constraint:the development, morphometrics, and behavioral basisof a fighter-flier polymorphism in male Hoplothrips karni(Insecta: Thysanoptera). Behav. Ecol. Sociobiol. 23,93–104. (doi:10.1007/BF00299892)

Cruickshank, T. & Wade, M. J. 2008 Microevolutionarysupport for a developmental hourglass: gene expressionpatterns shape sequence variation and divergence in

Drosophila. Evol. Dev. 10, 583–590. (doi:10.1111/j.1525-142X.2008.00273.x)

Darwin, C. 1871 The descent of man and selection in relation tosex. London, UK: John Murray.

Demuth, J. P. & Wade, M. J. 2007 Maternal expressionincreases the rate of bicoid evolution by relaxing selectiveconstraint. Genetica 129, 37–43. (doi:10.1007/s10709-006-0031-4)

Donnell, D. M. & Strand, M. R. 2006 Caste-based differ-

ences in gene expression in the polyembryonic waspCopidosoma floridanum. Ins. Biochem. Mol. Biol. 36,141–153. (doi:10.1016/j.ibmb.2005.11.009)

Dworkin, I. 2005 Canalization, cryptic variation, and devel-opmental buffering: a critical examination and analytical

perspective. In Variation—a central concept in biology(eds B. Hallgrı́msson & B. K. Hall), pp. 131–158.Burlington, USA: Elsevier/Academic Press.

Eberhard, W. G. 1985 Sexual selection and animal genitalia.Cambridge, MA: Harvard University Press.

Eberhard, W. G., Huber, B. A., Rodriguez, R. L., Briceno,R. D. & Rodriguez, V. 1998 One size fits all? Relationshipsbetween the size and degree of variation in genitalia andother body parts in twenty species of insects and spiders.

Evolution 52, 415–431. (doi:10.2307/2411078)Emlen, D. J. 1994 Environmental control of horn length

dimorphism in the beetle Onthophagus acuminatus(Coleoptera: Scarabaeidae). Proc. R. Soc. Lond. B 256,131–136. (doi:10.1098/rspb.1994.0060)

Emlen, D. J. 2000 Integrating development with evolution: acase study with beetle horns. Bioscience 50, 403–418.(doi:10.1641/0006-3568(2000)050[0403:IDWEAC]2.0.CO;2)

Emlen, D. J. & Nijhout, H. F. 1999 Hormonal control of

male horn length dimorphism in the dung beetle Ontho-phagus taurus (Coleoptera: Scarabaeidae). J. Ins. Physiol.45, 45–53. (doi:10.1016/S0022-1910(98)00096-1)

Evans, J. D. & Wheeler, D. E. 1999 Differential geneexpression between developing queens and workers in

the honey bee. Apis mellifera. Proc. Natl Acad. Sci. USA96, 5575–5580. (doi:10.1073/pnas.96.10.5575)

Evans, J. D. & Wheeler, D. E. 2001a Expressionprofiles during honeybee caste determination. GenomeBiol. 2, research0001.1-0001.6. (doi:10.1186/gb-2000-2-1-research0001).

Evans, J. D. & Wheeler, D. E. 2001b Gene expression andthe evolution of insect polyphenisms. Bioessays 23,62–68. (doi:10.1002/1521-1878(200101)23:1,62::AID-BIES1008.3.0.CO;2-7)

Gilbert, S. F. & Epel, D. 2009 Ecological developmentalbiology: integrating epigenetics, medicine, and evolution.Sunderland, MA: Sinauer.

Grimaldi, D. & Engel, M. S. 2005 Evolution of the insects.Cambridge, UK: Cambridge University Press.

Hoffman, E. A. & Goodisman, M. A. D. 2007 Geneexpression and the evolution of phenotypic diversityin social wasps. BMC Biol. 5, 23. (doi:10.1186/1741-7007-5-23)

Hojo, M., Koshikawa, S., Cornette, R., Matsumoto, T. &Miura, T. 2005 Identification of soldier-specific genes inthe nasute termite Nasutitermes takasagoensis (Isoptera:Termitidae). Ent. Sci. 8, 379–387. (doi:10.1111/j.1479-8298.2005.00138.x)

http://dx.doi.org/doi:10.1126/science.1071468http://dx.doi.org/doi:10.1371/journal.pgen.0010057http://dx.doi.org/doi:10.1371/journal.pgen.0010057http://dx.doi.org/doi:10.1086/374344http://dx.doi.org/doi:10.1007/BF00299892http://dx.doi.org/doi:10.1111/j.1525-142X.2008.00273.xhttp://dx.doi.org/doi:10.1111/j.1525-142X.2008.00273.xhttp://dx.doi.org/doi:10.1007/s10709-006-0031-4http://dx.doi.org/doi:10.1007/s10709-006-0031-4http://dx.doi.org/doi:10.1016/j.ibmb.2005.11.009http://dx.doi.org/doi:10.2307/2411078http://dx.doi.org/doi:10.1098/rspb.1994.0060http://dx.doi.org/doi:10.1641/0006-3568(2000)050[0403:IDWEAC]2.0.CO;2http://dx.doi.org/doi:10.1641/0006-3568(2000)050[0403:IDWEAC]2.0.CO;2http://dx.doi.org/doi:10.1016/S0022-1910(98)00096-1http://dx.doi.org/doi:10.1073/pnas.96.10.5575http://dx.doi.org/doi:10.1186/gb-2000-2-1-research0001http://dx.doi.org/doi:10.1186/gb-2000-2-1-research0001http://dx.doi.org/doi:10.1002/1521-1878(200101)23:1%3C62::AID-BIES1008%3E3.0.CO;2-7http://dx.doi.org/doi:10.1002/1521-1878(200101)23:1%3C62::AID-BIES1008%3E3.0.CO;2-7http://dx.doi.org/doi:10.1002/1521-1878(200101)23:1%3C62::AID-BIES1008%3E3.0.CO;2-7http://dx.doi.org/doi:10.1002/1521-1878(200101)23:1%3C62::AID-BIES1008%3E3.0.CO;2-7http://dx.doi.org/doi:10.1002/1521-1878(200101)23:1%3C62::AID-BIES1008%3E3.0.CO;2-7http://dx.doi.org/doi:10.1002/1521-1878(200101)23:1%3C62::AID-BIES1008%3E3.0.CO;2-7http://dx.doi.org/doi:10.1002/1521-1878(200101)23:1%3C62::AID-BIES1008%3E3.0.CO;2-7http://dx.doi.org/doi:10.1186/1741-7007-5-23http://dx.doi.org/doi:10.1186/1741-7007-5-23http://dx.doi.org/doi:10.1111/j.1479-8298.2005.00138.xhttp://dx.doi.org/doi:10.1111/j.1479-8298.2005.00138.xhttp://rstb.royalsocietypublishing.org/



Hölldobler, B. & Wilson, E. O. 1990 The ants. Berlin,Germany: Springer.

Holt, R. D. 1996 Demographic constraints in evolution:

towards unifying the evolutionary theories of senescenceand niche conservatism. Evol. Ecol. 6, 433–447.(doi:10.1007/BF02270702)

Howden, H. F. & Young, O. P. 1981 Panamanian Scarabaei-nae: taxonomy, distribution, and habits (Coleoptera:

Scarabaeidae). Contr. Am. Ent. Inst. 18, 1–204.Jacobs, W. & Renner, M. 1988 Biologie und Ökologie der

Insekten. Stuttgart, Germany: Gustav Fischer.Judice, C. C., Carazzole, M. F., Festa, F., Sogayar, M. C.,

Hartfelder, K. & Pereira, G. A. G. 2006 Gene expressionprofiles underlying alternative caste phenotypes in ahighly eusocial bee, Melipona quadrifasciata. Ins. Mol.Biol. 15, 33–44. (doi:10.1111/j.1365-2583.2005.00605.x)

Klingenberg, C. P. & Nijhout, H. F. 1998 Competition

among growing organs and developmental control ofmorphological asymmetry. Proc. R. Soc. Lond. B 265,1135–1139. (doi:10.1098/rspb.1998.0409)

Kutsukake, M., Shibao, H., Nikoh, N., Morioka, M.,Tamura, T., Hoshino, T., Ohgiya, S. & Fukatsu, T.

2004 Venomous protease of aphid soldier for colonydefense. Proc. Natl Acad. Sci. USA 101, 11 338–11 343.(doi:10.1073/pnas.0402462101)

Lüscher, M. 1960 Hormonal control of caste differentiationin termites. Ann. N. Y. Acad. Sci. 89, 549–563. (doi:10.1111/j.1749-6632.1960.tb27577.x)

Matthews, E. G. 1972 A revision of the scarabaeinaedung beetles of Australia. I. Tribe Onthophagini.Austr. J. Zool. Suppl. Ser. 9, 1–330.

Moczek, A. P. 2003 The behavioral ecology of thresholdevolution in a polyphenic beetle. Behav. Ecol. 14,831–854. (doi:10.1093/beheco/arg062)

Moczek, A. P. 2005 The evolution and development ofnovel traits, or how beetles got their horns. BioScience11, 935–951.

Moczek, A. P. 2008 On the origin of novelty in developmentand evolution. Bioessays 5, 432–447. (doi:10.1002/bies.20754)

Moczek, A. P. 2009 Developmental plasticity and the

origins of diversity: a case study on horned beetles. InPhenotypic plasticity in insects: mechanisms and consequences(T. N. Ananthakrishnan & D. Whitman), pp. 81–134.Plymouth, UK: Science Publishers.

Moczek, A. P. & Emlen, D. J. 2000 Male horn dimorphism

in the scarab beetle Onthophagus taurus: do alternativereproductive tactics favor alternative phenotypes? Anim.Behav. 59, 459–466. (doi:10.1006/anbe.1999.1342)

Moczek, A. P. & Nijhout, H. F. 2002 Developmental

mechanisms of threshold evolution in a polyphenicbeetle. Evol. Dev. 4, 252–264. (doi:10.1046/j.1525-142X.2002.02014.x)

Moczek, A. P. & Nijhout, H. F. 2003 Rapid evolution of apolyphenic threshold. Evol. Dev. 5, 259–268. (doi:10.1046/j.1525-142X.2003.03033.x)

Moczek, A. P. & Nijhout, H. F. 2004 Trade-offs during thedevelopment of primary and secondary sexual traits in ahorn dimorphic beetle. Am. Nat. 163, 184–191.(doi:10.1086/381741)

Moczek, A. P., Hunt, J., Emlen, D. J. & Simmons, L. W. 2002Evolution of a developmental threshold in exotic popu-lations of a polyphenic beetle. Evol. Ecol. Rev. 4, 587–601.

Moczek, A. P., Cruickshank, T. E. & Shelby, J. A. 2006When ontogeny reveals what phylogeny hides: gain and

loss of horns during development and evolution ofhorned beetles. Evolution 60, 2329–2341.

Moran, N. A. 1991 Phenotype fixation and genotypic diver-sity in the complex life cycle of the aphid Pemphigus betae.Evolution 45, 957–970. (doi:10.2307/2409702)


Nijhout, H. F. 1994 Insect hormones. Princeton, NJ:Princeton University Press.

Nijhout, H. F. 1999 Control mechanisms of polyphenic

development in insects. BioScience 49, 181–192.(doi:10.2307/1313508)

Nijhout, H. F. 2003 Development and evolution of adaptivepolyphenisms. Evol. Dev. 5, 9–18. (doi:10.1046/j.1525-142X.2003.03003.x)

Nijhout, H. F. & Emlen, D. J. 1998 Competition amongbody parts in the development and evolution of insectmorphology. Proc. Natl Acad. Sci. USA 95, 3685–3689.(doi:10.1073/pnas.95.7.3685)

Parzer, H. F. & Moczek, A. P. 2008 Rapid antagonisticcoevolution between primary and secondary sexual char-acters in horned beetles. Evolution 62, 2423–2428.(doi:10.1111/j.1558-5646.2008.00448.x)

Pereboom, J. J. M., Jordan, W. C., Sumner, S., Hammond,

R. L. & Bourke, A. G. F. 2005 Differential geneexpression in queen-worker caste determination inbumble-bees. Proc. R. Soc. B 272, 1145–1152. (doi:10.1098/rspb.2005.3060)

Pigliucci, M. 2001 Phenotypic plasticity. Baltimore, MD:Johns Hopkins University Press.

Pizzo, A., Roggero, A., Palestrini, C., Moczek, A. P. &Rolando, A. 2008 Rapid shape divergences between

natural and introduced populations of a horned beetlepartly mirror divergences between species. Evol. Dev.10, 166–175.

Scharf, M. E., Wu-Scharf, D., Pittendrigh, B. R. & Bennett,G. W. 2003 Caste- and development-associated geneexpression in a lower termite. Genome Biol. 4, R62.(doi:10.1186/gb-2003-4-10-r62)

Scharloo, W. 1991 Canalization: genetic and developmentalaspects. Ann. Rev. Ecol. Syst. 22, 65–93. (doi:10.1146/annurev.es.22.110191.000433)

Schlichting, C. D. & Pigliucci, M. 1995 Gene regulation,

quantitative genetics, and the evolution of reaction norms.Evol. Ecol. 9, 154–168. (doi:10.1007/BF01237754)

Schlichting, C. D. & Pigliucci, M. 1998 Phenotypic evolution:a reaction norm perspective. Sunderland, MA: Sinauer.

Shapiro, A. M. 1976 Seasonal polyphenism. Evol. Biol. 9,259–333.

Shepherd, B. L., Prange, H. D. & Moczek, A. P. 2008 Somelike it hot: body and weapon size affect thermoregulationin horned beetles. J. Ins. Physiol. 54, 604–611. (doi:10.1016/j.jinsphys.2007.12.007)

Simmons, L. W. & Emlen, D. J. 2006 Evolutionary trade-offbetween weapons and testes. Proc. Natl Acad. Sci. USA103, 16 346–16 351. (doi:10.1073/pnas.0603474103)

Snell-Rood, E. C. & Moczek, A. P. In press. Horns, hor-

mones, and hox genes: the role of development in theevolution of beetle contests. In Animal contests (edsI. C. W. Hardy & M. Briffa), Cambridge, UK: CambridgeUniversity Press.

Snell-Rood, E. C. & Papaj, D. R. 2009 Patterns of phenotyp-

ic plasticity in common and rare environments: a study ofhost use and color learning in the cabbage white butterflyPieris rapae. Am. Nat. 173, 615–631. (doi:10.1086/597609)

Snell-Rood, E. C., Papaj, D. R. & Gronenberg, W. 2009

Brain size: a global or induced cost of learning? BrainBehav. Evol. 73, 111–128. (doi:10.1159/000213647)

Snell-Rood, E. C., Van Dyken, J. D., Cruickshank, T. E.,Wade, M. J. & Moczek, A. P. In press a. Toward a popu-lation genetic framework of developmental evolution:

costs, limits, and consequences of phenotypic plasticity.Bioessays.

Snell-Rood, E. C., Davidowitz, G. & Papaj, D. R. In press b.Reproductive delays are linked to learning ability ina butterfly. Behav. Ecol.

http://dx.doi.org/doi:10.1007/BF02270702http://dx.doi.org/doi:10.1111/j.1365-2583.2005.00605.xhttp://dx.doi.org/doi:10.1098/rspb.1998.0409http://dx.doi.org/doi:10.1073/pnas.0402462101http://dx.doi.org/doi:10.1111/j.1749-6632.1960.tb27577.xhttp://dx.doi.org/doi:10.1111/j.1749-6632.1960.tb27577.xhttp://dx.doi.org/doi:10.1093/beheco/arg062http://dx.doi.org/doi:10.1002/bies.20754http://dx.doi.org/doi:10.1002/bies.20754http://dx.doi.org/doi:10.1006/anbe.1999.1342http://dx.doi.org/doi:10.1046/j.1525-142X.2002.02014.xhttp://dx.doi.org/doi:10.1046/j.1525-142X.2002.02014.xhttp://dx.doi.org/doi:10.1046/j.1525-142X.2003.03033.xhttp://dx.doi.org/doi:10.1046/j.1525-142X.2003.03033.xhttp://dx.doi.org/doi:10.1086/381741http://dx.doi.org/doi:10.2307/2409702http://dx.doi.org/doi:10.2307/1313508http://dx.doi.org/doi:10.1046/j.1525-142X.2003.03003.xhttp://dx.doi.org/doi:10.1046/j.1525-142X.2003.03003.xhttp://dx.doi.org/doi:10.1073/pnas.95.7.3685http://dx.doi.org/doi:10.1111/j.1558-5646.2008.00448.xhttp://dx.doi.org/doi:10.1098/rspb.2005.3060http://dx.doi.org/doi:10.1098/rspb.2005.3060http://dx.doi.org/doi:10.1186/gb-2003-4-10-r62http://dx.doi.org/doi:10.1146/annurev.es.22.110191.000433http://dx.doi.org/doi:10.1146/annurev.es.22.110191.000433http://dx.doi.org/doi:10.1007/BF01237754http://dx.doi.org/doi:10.1016/j.jinsphys.2007.12.007http://dx.doi.org/doi:10.1016/j.jinsphys.2007.12.007http://dx.doi.org/doi:10.1073/pnas.0603474103http://dx.doi.org/doi:10.1086/597609http://dx.doi.org/doi:10.1086/597609http://dx.doi.org/doi:10.1159/000213647http://rstb.royalsocietypublishing.org/



Stern, D. L. & Foster, W. A. 1996 The evolution of soldiersin aphids. Biol. Rev. 71, 27–79. (doi:10.1111/j.1469-185X.1996.tb00741.x)

Tauber, M. J. & Tauber, C. A. 1972 Geographic variation incritical photoperiod and in diapause intensity of Chrysopacarnea (Neuroptera). J. Ins. Physiol. 18, 25–29. (doi:10.1016/0022-1910(72)90061-3)

Van Dyken, J. D. & Wade, M. J. In press. On the

evolutionary genetics of conditionally expressed genes.Genetics.

Via, S., Gomulkiewicz, R., de Jong, G., Scheiner, S. M.,Schlichting, C. D. & Van Tienderen, P. 1995 Adaptive

phenotypic plasticity: consensus and controversy. TrendsEcol. Evol. 10, 212–217. (doi:10.1016/S0169-5347(00)89061-8)

Wade, M. J. 1998 The evolutionary genetics of maternaleffects. In Maternal effects as adaptations (eds T. A.Mousseau & C. W. Fox), pp. 5–21. Oxford, UK:Oxford University Press.

West-Eberhard, M. J. 2003 Developmental plasticity andevolution. New York, NY: Oxford University Press.


Wheeler, D. E. & Nijhout, H. F. 1983 Soldier determinationin Pheidole bicarinata: effect of methophrene on caste andsize within castes. J. Ins. Physiol. 29, 847–854. (doi:10.1016/0022-1910(83)90151-8)

Wheeler, D. E. & Nijhout, H. F. 1984 Soldier determinationin the ant Pheidole bicarinata: inhibition by adult soldiers.J. Ins. Physiol. 30, 127–135. (doi:10.1016/0022-1910(84)90116-1)

Wilson, E. O. 1953 The origin and evolution of polymorph-ism in ants. Quart. Rev. Biol. 28, 136–156. (doi:10.1086/399512)

Wilson, E. O. 1976 Behavioral discretization and the number

of castes in an ant species. Behav. Ecol. Sociobiol. 1,141–154. (doi:10.1007/BF00299195)

Yang, A. S. 2001 Modularity, evolvability, and adaptive radi-ations: a comparison of the hemi- and holometabolousinsects. Evol. Dev. 2, 59–72. (doi:10.1046/j.1525-142x.2001.003002059.x)

Zera, A. J. & Denno, R. F. 1997 Physiology and ecology ofdispersal polymorphism in insects. Ann. Rev. Entomol.42, 207–231. (doi:10.1146/annurev.ento.42.1.207)

http://dx.doi.org/doi:10.1111/j.1469-185X.1996.tb00741.xhttp://dx.doi.org/doi:10.1111/j.1469-185X.1996.tb00741.xhttp://dx.doi.org/doi:10.1016/0022-1910(72)90061-3http://dx.doi.org/doi:10.1016/0022-1910(72)90061-3http://dx.doi.org/doi:10.1016/S0169-5347(00)89061-8http://dx.doi.org/doi:10.1016/S0169-5347(00)89061-8http://dx.doi.org/doi:10.1016/0022-1910(83)90151-8http://dx.doi.org/doi:10.1016/0022-1910(83)90151-8http://dx.doi.org/doi:10.1016/0022-1910(84)90116-1http://dx.doi.org/doi:10.1016/0022-1910(84)90116-1http://dx.doi.org/doi:10.1086/399512http://dx.doi.org/doi:10.1086/399512http://dx.doi.org/doi:10.1007/BF00299195http://dx.doi.org/doi:10.1046/j.1525-142x.2001.003002059.xhttp://dx.doi.org/doi:10.1046/j.1525-142x.2001.003002059.xhttp://dx.doi.org/doi:10.1146/annurev.ento.42.1.207http://rstb.royalsocietypublishing.org/

Phenotypic plasticity and diversity in insectsIntroductionPhenotypic plasticity—ubiquitous yet limitedInsect biology and the range and power of plasticityHorned beetles: a microcosm for understanding the causes, mechanisms and consequences of plasticity

Phenotypic plasticity and organismal diversificationPhenotypic plasticity provides novel targets for evolutionary processesPhenotypic plasticity creates novel trade-offsPhenotypic plasticity increases genetic variation and divergence—the mutation-modularity trade-off hypothesis

ConclusionsTami Cruickshank and Emilie Snell-Rood provided helpful comments on earlier drafts of this chapter. Research presented here was supported by National Science Foundation grants IOS 0445661 and IOS 0718522.References

Phenotypic plasticity and diversity in insects plasticity and diversity in insects.pdfPhenotypic...

Documents

Transcript of Phenotypic plasticity and diversity in insects plasticity and diversity in insects.pdfPhenotypic...